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Vol. 19: 297–305, 2013 AQUATIC BIOLOGY Published online November 11 doi: 10.3354/ab00539 Aquat Biol Shell morphology and genetic characteristics of Corbula (Potamocorbula) spp. (Bivalvia: Corbulidae) from the waters adjacent to Japan, Korea and San Francisco Bay Masato Owada1,*, Yoshitaro Kasai2, Shin’ichi Sato3, Jae-Sang Hong4 1Department of Biological Sciences, Kanagawa University, 2946 Tsuchiya, Hiratsuka 259-1293, Japan 2Department of Earth Sciences, Graduate School of Science, Tohoku University, 6-3 Aoba, Aramaki, Aoba-ku, Sendai 980-8578, Japan 3The Tohoku University Museum, 6-3 Aoba, Aramaki, Aoba-ku, Sendai 980-8578, Japan 4Department of Oceanography, Inha University, Incheon 402-751, South Korea ABSTRACT: Corbula (Potamocorbula) spp. are natively distributed in the waters adjacent to Japan and Korea. These populations are distinguished by 6 morphological characteristics. How- ever, they have high geographic variation, and it is quite difficult to distinguish among them. In the present study, we investigated the geographic distribution of the morphological and genetic characteristics of Corbula (Potamocorbula) spp. collected from the waters adjacent to Japan, Korea and San Francisco Bay, USA. Shell morphology was inferred through canonical discrimi- nant analysis (CDA) of 8 shell characteristics, and genetic characteristics were analysed using the DNA sequences of mitochondrial cytochrome c oxidase subunit 1 (CO1) and nuclear internal tran- scribed spacer 2 (ITS2) regions. The results of CDA showed that the samples from Ganghwa-do in western Korea could be clearly separated from those of all the other localities. The molecular phy- logenetic tree and haplotype network that were constructed from the CO1 and ITS2 regions, respectively, did not show clear groupings among the collected samples, except for 1 group com- posed of samples from Ganghwa-do. In addition, no differences in CO1 amino acid sequences could be found among any of the samples examined, including the Ganghwa-do samples. These facts suggest that Corbula (Potamocorbula) spp. distributed in the waters adjacent to Japan and Korea were separated into 2 groups. However, these 2 groups were genetically closely related, and it seems appropriate to treat them as 2 distinct species. The classification of the subgenus Potamocorbula should be re-examined at the species level. KEY WORDS: Mollusca · Bivalvia · Corbulidae · Potamocorbula · Phylogeography · Classification · Mitochondrial cytochrome c oxidase subunit 1 · Nuclear internal transcribed spacer 2 Resale or republication not permitted without written consent of the publisher INTRODUCTION East Asia (Carlton et al. 1990, Nichols et al. 1990). It is known that the waters adjacent to Japan and Populations of the Asian (overbite) clam, Corbula Korea in the Northwest Pacific are inhabited by at (Potamocorbula) amurensis Schrenck, 1861, in San least 4 species of the subgenus Potamocorbula Habe, Francisco Bay, USA, have markedly increased since 1955. These species are distinguishable from each 1986. They were introduced to the region through other by 6 morphological characteristics: shell size, ballast waters from a cargo ship that had stopped in shell outline, shell inflation, shell thickness, posterior *Email: [email protected] © Inter-Research 2013 · www.int-res.com 298 Aquat Biol 19: 297–305, 2013 margin and position of the umbo (Zhuang & Cai 1983, DNA. However, they did not simultaneously discuss Habe 1994, Horikoshi & Okamoto 1994, Tsuchida & the relationships between the morphological and Okamura 1997). However, Sato (2002, 2005) and Sato genetic characteristics. In the present study, we & Kanazawa (2004) reported that there were high investigated the geographic distribution of the mor- geographic variations in these morphological charac- phological and genetic characteristics of the popula- teristics, making it challenging to distinguish among tions from the waters adjacent to Japan, Korea and these species. San Francisco Bay through canonical discriminant Corbula (Potamocorbula) amurensis is regarded as analysis (CDA) of 8 shell characteristics and through an invasive species in San Francisco Bay and may the DNA sequences of mitochondrial cytochrome c have a significant impact on the estuarine ecosystem oxidase subunit 1 (CO1) and nuclear internal tran- of the bay (Carlton 1999, Coan 2002, Kimmerer 2002, scribed spacer 2 (ITS2) regions. Greene et al. 2011). In addition, fossil specimens of this species have been used as indicators of a cool cli- mate or brackish water during reconstructions of the MATERIALS AND METHODS paleoenvironments of the Late Pleistocene and Holocene in Japan (Matsushima 1984, Habe 1994). Sampling However, these may not be accurate until the rela- tionships between the geographic distribution and Corbula (Potamocorbula) spp. were collected from morphological characteristics of Corbula (Potamocor- 8 localities shown in Fig. 1: Rokkaku River Estuary, bula) spp. are fully understood at both population Saga Prefecture, Ariake Sea, western Japan (N = 25 and species levels. To clarify the relationships among individuals collected on 12 July 1998 and 23 Novem- members of Corbula (Potamocorbula) spp., it will be ber 2008); Dong River Estuary, Suncheon-si, south- necessary to investigate the morphological and ern Korea (N = 30, 20 August 2011); Mangyeong genetic characteristics of populations from various River Estuary, Gunsan-si, western Korea (N = 30, 3 localities. There have been several discussions of the May 2000 and 11 July 2008); Ganghwa-do, intertidal genetic characteristics of Corbula (Potamocorbula) muddy sand flat, western Korea (N = 30, 8 May 1998 spp. For example, Duda (1994) reported that C. (P.) and 18 August 2011); Maeho Lake, Yangyang-gun, amurensis from San Francisco Bay, California, shows eastern Korea (N = 30, 16 July 2008); Hinuma Lake, high genetic variation. Further, Smith et al. (2012) Ibaraki Prefecture, central Japan (N = 30, 31 May indicated that C. (P.) amurensis from San Francisco 1998 and 30 July 2011); Obuchi Swamp, Aomori Pre- Bay and the Ariake Sea, western Japan, can be iden- fecture, northern Japan (N = 46, 3 September 1998 tified using the same genetic marker, 18S ribosomal and 27 July 2009); and San Francisco Bay, California, 45° 45° N N USA Os Pacific Japan / East Ocean Sea Sf Seoul Ml Gd San Francisco South Japan Yellow Mr Hl Sea Korea 35° Tokyo 35° Dr Pacific Ocean Rr 200 km 200 km 130°E 140° 130°W 120° Fig. 1. Localities where the samples were collected. Rr: Rokkaku River Estuary (33°11’ N, 130°12’ E); Dr: Dong River Estuary (34° 51’ N, 127° 30’ E); Mr: Mangyeong River Estuary (35° 51’ N, 126° 40’ E); Gd: Ganghwa-do (37° 36’ N, 126° 22’ E); Ml: Maeho Lake (37° 56’ N, 128° 46’ E); Hl: Hinuma Lake (36° 16’ N, 140° 30’ E); Os: Obuchi Swamp (40° 57’ N, 141° 22’ E); Sf: San Francisco Bay (37° 27’ N, 122° 1’ W) Owada et al.: Morphological and genetic characteristics of Corbula (Potamocorbula) spp. 299 USA (N =30, 9 February 2000 and 9 November 2010). Polymerase chain reaction (PCR) In addition, C. (P.) fasciata and Solidicorbula ery- throdon, which were used as outgroups in the ana - CO1 and ITS2 regions were amplified using Pre- lysis of genetic variation, were collected from Bohol mix Taq (Takara) and a PCR Thermal Cycler PER- Island in the Philippines (9°44’ N, 123°53’ E) on 8 SONAL (Takara). The following primers were newly June 2007 and from Sagami Bay in Japan (35°17’ N, designed for the present study: 5′-TCW ACA AAT 139°20’ E) on 7 September 2011, respectively. The CAY AAA GAT ATT GG-3′ (forward) and 5′-ACY soft tissue of living animals was preserved in 100% TCM GGR TGM CCA AAA AAT CA-3′ (reverse) for ethanol, and DNA was extracted from the foot or the CO1 region, and 5′-ATT GCA GGA CAC ATT adductor muscle using the DNeasy Blood & Tissue GAA CAT CG-3′ (forward) and 5′-GTT ACT GAG Kit (Qiagen). The shell and soft tissue were num- GGA ATC CTT GTT A-3′ (reverse) for the ITS2 bered in each individual. All voucher samples were region. The conditions for PCR amplification were as deposited in the Tohoku University Museum (TUMC follows: denaturation at 94°C for 30 s, annealing at Nos. 111200 to 111207). 54°C for 30 s (CO1) and 55°C for 30 s (ITS2) and extension at 72°C for 60 s. These steps were repeated 30 times. The PCR products were purified using Morphological analysis ExoSAP-IT (USB), and cycle-sequencing reactions were performed using BigDye Terminator Version Eight shell characteristics (in mm): shell length 3.1 Cycle Sequencing Kit (ABI PRISM). The se - (L), shell breadth (B), shell height of left valve (HL), quences were compiled using a 3130 Genetic Ana- shell height of right valve (HR), thickness of shell lyzer (ABI PRISM) from both the 5′ and 3′ directions. margin (T), height of umbo (U), posterior shell These sequences were registered in the DNA Data length (PL) and upper shell height (UH) were meas- Bank of Japan (CO1: AB740093 to AB740137 and ured on each individual (Fig. 2). For measurement AB 827932 to AB827935, ITS2: AB740177 to AB740218 of L, HR, U, PL and UH, the outside of the right shell and AB827936 to AB827938). valve was photographed with a digital camera, and then each characteristic was measured using image analysis software, ImageJ ver. 1.45s. Further, L, B, Genetic analysis HL, HR and T were measured using a digital slide caliper (accuracy ± 0.01 mm). L and HR were meas- In the analysis of genetic variation in the CO1 re- ured using both methods, but there were no signifi- gion, the sequences of Varicorbula dissimilis (AF cant differences (p > 0.05) between them. Then, to 120669), Solidicorbula erythrodon (AB740137), and standardize the variability for size, all characteristics Corbula (Potamocorbula) fasciata (AB740136) were were log-transformed (using base 10 logs), and the included as outgroups. After alignment using Clustal 7 characteristics excluding L were divided by the W Version 1.8 (Thompson et al.
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    Palaeontologia Electronica http://palaeo-electronica.org ROLE OF CONSTRAINT AND SELECTION IN THE MORPHOLOGIC EVOLUTION OF CARYOCORBULA (MOLLUSCA: CORBULIDAE) FROM THE CARIBBEAN NEOGENE Laurie C. Anderson and Peter D. Roopnarine ABSTRACT We examined patterns of morphologic evolution in Caryocorbula, a common bivalve genus of the Caribbean Neogene, to evaluate the roles that constraint and selection play in its apparent morphologic conservatism. With multivariate analyses using landmark-based geometric morphometrics, we examined the relationship of valve size and outline shape within the Caryocorbula + (Bothrocorbula + Hexacorbula) clade, and within 21 morphospecies of Caryocorbula, all from Neogene deposits of the Caribbean region. We found that each genus is morphologically distinct both in shape and size, and that Caryocorbula shows strong interspecific allometry that persists despite species turnover and the vagaries of geographic and temporal sample cover- age. Persistence of this allometric trend indicates that constraints shape Caryocorbula morphology. Constraint mechanisms may relate to 1) space limitations in the inequiva- lved shells that characterize Corbulidae, and/or 2) the need for functional articulation of unequal valves through a complex shell accretion history. Alternatively, environmental conditions, particularly nutrient availability, may control the spatial and temporal distri- bution of large Caryocorbula, but constraint via pleiotropy could restrict the shape of these bivalves. Finally, although constraints appear to play an important role in the morphologic evolution of Neogene Caryocorbula, an adaptive relationship of size and shape to environment is not precluded, as illustrated for Caryocorbula species from the late Miocene-early Pliocene of the northern Dominican Republic. The morphology of these species falls along the interspecific allometric curve, but each is also characteris- tic of a particular paleoenvironmental setting, with valve size and shape tracking with inferred depth and physical energy gradients.